MBE Advance Access originally published online on October 19, 2005
Molecular Biology and Evolution 2006 23(2):365-371; doi:10.1093/molbev/msj042
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Research Article |
Genome Plasticity and ori-ter Rebalancing in Salmonella typhi
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,1,
* Department of Microbiology, Peking University Health Science Center, Beijing, China; Department of Microbiology and Infectious Diseases, University of Calgary, Calgary, Alberta, Canada; Department of Microbiology, Harbin Medical University, Harbin, China; Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada; and || Department of Biochemistry and Molecular Biology, University of Calgary, Calgary, Alberta, Canada
E-mail: slliu{at}bjmu.edu.cn.
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Abstract |
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 TOP Abstract IntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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Genome plasticity resulting from frequent rearrangement of the bacterial genome is a fascinating but poorly understood phenomenon. First reported in Salmonella typhi, it has been observed only in a small number of Salmonella serovars, although the over 2,500 known Salmonella serovars are all very closely related. To gain insights into this phenomenon and elucidate its roles in bacterial evolution, especially those involved in the formation of particular pathogens, we systematically analyzed the genomes of 127 wild-type S. typhi strains isolated from many places of the world and compared them with the two sequenced strains, Ty2 and CT18, attempting to find possible associations between genome rearrangement and other significant genomic features. Like other host-adapted Salmonella serovars, S. typhi contained large genome insertions, including the 134 kb Salmonella pathogenicity island, SPI7. Our analyses showed that SPI7 disrupted the physical balance of the bacterial genome between the replication origin (ori) and terminus (ter) when this DNA segment was inserted into the genome, and rearrangement in individual strains further changed the genome balance status, with a general tendency toward a better balanced genome structure. In a given S. typhi strain, genome diversification occurred and resulted in different structures among cells in the culture. Under a stressed condition, bacterial cells with better balanced genome structures were selected to greatly increase in proportion; in such cases, bacteria with better balanced genomes formed larger colonies and grew with shorter generation times. Our results support the hypothesis that genome plasticity as a result of frequent rearrangement provides the opportunity for the bacterial genome to adopt a better balanced structure and thus eventually stabilizes the genome during evolution.
Key Words: Salmonella typhi • genome plasticity • ori-ter rebalancing • I-CeuI • genome rearrangements • typhoid
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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Physical structure of the bacterial genome has been known to be highly conservative during evolution in many cases such as in Escherichia coli and Salmonella, in which genomic comparisons were possible by linkage analysis (Taylor and Thoman 1964
; Sanderson and Demerec 1965), physical mapping (Kohara, Akiyama, and Isono 1987; Smith et al. 1987; Liu and Sanderson 1992; Wong and McClelland 1992), and sequencing (McClelland et al. 2001, 2004; Parkhill et al. 2001; Deng et al. 2003). Escherichia coli and Salmonella have diverged for over 100 MYR (Ochman and Wilson 1987; Doolittle et al. 1996; Feng, Cho, and Doolittle 1997) but their genome structures remain highly similar (Krawiec and Riley 1990; Liu, Hessel, and Sanderson 1993). Within Salmonella, the conservation is even higher: strains across all eight major Salmonella subgroups usually have a common genome structure (Liu et al. 1999). However, a small number of Salmonella serovars are puzzling exceptions in that they have remarkably diverse genome structures, with the DNA segments being rearranged in many different ways, as observed in Salmonella typhi (Liu and Sanderson 1996; Kothapalli et al. 2005) and some other host-adapted Salmonella pathogens (Liu and Sanderson 1998; Liu et al. 2003). We speculated that rearrangements leading to genome plasticity in these bacteria might reflect or contribute to some special evolutionary processes in the creation of new pathogens.
Previously, in an attempt to correlate genome rearrangement with any other genomic features for clues that might give insights into the phenomenon, we compared the genome maps between S. typhi and other Salmonella serovars that have stable genomes. Most outstanding of the few extraordinary genomic features that we found in S. typhi was a large insertion (Liu and Sanderson 1995b), later identified as Salmonella pathogenicity island SPI7 with a size of 134 kb (Parkhill et al. 2001; Nair et al. 2004). We postulated that this insertion, while presumably conferring phenotypic benefits to the bacteria, would nevertheless disrupt the physical balance of the circular genome between origin (ori) and terminus (ter) of DNA replication, delaying the completion of DNA replication cycles and slowing the bacterial growth (Liu and Sanderson 1995b, 1995d). Based on this postulation, we hypothesized that a physical balance between ori and ter would normally exist on the bacterial genome for simultaneous completion of DNA replication in the two directions, and rearrangement of genomic DNA segments would help reestablish the balance once it is disrupted (Liu and Sanderson 1995d). The first half of this hypothesis has gained substantial support from genomic sequence analyses in numerous bacteria, such as Haemophilus influenzae Rd (Fleischmann et al. 1995), E. coli K12 (Blattner et al. 1997), Salmonella typhimurium LT2 (McClelland et al. 2001), and Salmonella paratyphi A (McClelland et al. 2004), which all have the circular genome divided into equal halves by ori and ter. Consistent with the hypothesis, bacteria with a balanced genome do not exhibit rearrangement, as demonstrated by a uniform genome structure among populations of S. typhimurium (Liu and Sanderson 1995c) and of S. paratyphi A (Liu and Sanderson 1995a). Wavelet analysis also reveals a general tendency of the bacterial genomes toward a physical balance between ori and ter (Song, Ware, and Liu 2003). On the other hand, the sequenced S. typhi strains indeed have unbalanced genomes (Parkhill et al. 2001; Deng et al. 2003) as predicted (Liu and Sanderson 1995d, 1996; Liu et al. 1999). In this study, we test the second half of the hypothesis, that is, genome plasticity is a result of rearrangement, which occurs in bacteria with unbalanced genomes and plays a key role in rebalancing the bacterial genome.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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Bacterial Strains
A total of 127 wild-type strains were analyzed in this study, including the reference strains Ty2 and CT18 (table 1). These strains were stocked at the Salmonella Genetic Stock Center, and strain information can be obtained at http://www.ucalgary.ca/
kesander/ or from the author.
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Isolation, Endonuclease Cleavage, and Electrophoresis Separation of Bacterial Genomic DNA
Bacteria were embedded in agarose for DNA isolation to avoid the shearing force to break the genome, as described previously (Liu et al. 2002
). Endonuclease cleavage with I-CeuI and AvrII and separation of the cleavage fragments by pulsed field gel electrophoresis were also described previously (Liu, Hessel, and Sanderson 1993; Liu and Sanderson 1995b).
Mapping of ori and ter on the Genome of S. typhi Strains
Genome maps were made for S. typhi wild-type strains by the procedure as reported (Liu and Sanderson 1995b, 1995d, 1996) and compared with those of Ty2 (Liu and Sanderson 1995b; Deng et al. 2003) and CT18 (Parkhill et al. 2001). Locations of ori and ter were determined for S. typhi strains based on their physical distances to the conservative endonuclease cleavage sites, movements of which resulting from rearrangements could be revealed by comparison with Ty2 or CT18. Specifically, location of ori can easily be determined by its proximity to rrnC, which can be conveniently localized by I-CeuI, and this physical distance is highly conservative in all sequenced Salmonella and E. coli strains. In contrast, ter covers a rather broad genomic region, including terA, terB, terC, terD, terE, terF, etc, and others such as tus and dif. Our work requires an accurate site of DNA replication termination for calculating the genome balance status. In Ty2, a site in the ter region that is 1,544 kb clockwise from thr is where the C/G distribution switches polarity (Deng et al. 2003); we used this site as ter in the analysis of the wild-type S. typhi strains in this study.
Transcytosis to Select for S. typhi Cells with Better Balanced Genomes
The procedures were described by Finlay et al. (Finlay and Falkow 1990). Briefly, S. typhi cells were inoculated on top of Caco2 human intestine cell monolayer, which had been grown at 37°C in RPMI 1640 supplemented with 10% fetal calf serum with 5% CO2 on the mesh of transwell culture plates (Finlay and Falkow 1990). Periodically, tissue culture medium beneath the monolayer was sampled by spreading onto Luria-Bertani (LB) agar plates to detect the existence and number of bacteria that had passed through the Caco2 cell monolayer.
Growth Rates of S. typhi Strains
Bacterial cells were grown in LB broth overnight at 37°C with vigorous shaking. This overnight culture was 1:2000 diluted and transferred to Klett flasks. Following incubation for 1 h, the culture was further 1:100 diluted and optical density (OD) reading was taken immediately. After every 10 min, the OD reading was taken until the stationary phase was reached. The growth rates were calculated according to the OD readings, expressed as Klett units, with one Klett unit being equivalent to 106 cells. The generation time was determined by comparing bacterial cell numbers at two time points of the exponential growth phase. When the Klett units expressed as log cell numbers and the times (in minutes) of the readings were plotted on a semilogarithmic graph, generation time of the bacteria was calculated by the formula:
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Results |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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Mapping of ori and ter in Populations of S. typhi
We first needed to know the genome balance status of the bacteria in different populations of S. typhi in order to further examine a correlation between genomic imbalance and rearrangement. Taking advantage of S. typhi for its highly conserved endonuclease cleavage sites and thus efficient point-to-point genomic comparisons among the strains, we mapped ori and ter for 125 S. typhi isolates through comparison with the sequenced S. typhi genomes (Parkhill et al. 2001
; Deng et al. 2003). The overall genome structure had first been determined by the I-CeuI technique (Liu and Sanderson 1996) and ambiguities of the orientations of I-CeuI A and C clarified by long range polymerase chain reaction (Kothapalli et al. 2005). We used AvrII in most cases to locate ori and ter in these strains, occasionally confirming the locations by XbaI or SpeI. Figure 1 shows the AvrII cleavage patterns of S. typhi strains Ty2 and CT18 (fig. 1A) and their genome structures shown as linear maps for a more convenient comparison (fig. 1B). In Ty2, ori is 3,750 kb clockwise from thrL (arbitrarily used as 0 kb) and ter is 1,544 kb from thrL (between narY and ansP). The genome size of Ty2 is 4,792 kb, so ori to ter clockwise is 2,586 kb or 194° and counterclockwise is 2,206 kb or 166°, leading to the ori-ter physical distances 14° off balance. CT18 has a similar AvrII cleavage pattern, with four apparent banding differences compared with Ty2 (fig. 1A) as a result of DNA rearrangements in rrn operons (fig. 1B). The inversion of I-CeuI A fragment in CT18 relative to Ty2 brings ter from 1,544 kb to the 1,435 kb position (fig. 1B), making the genome better balanced.
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DNA concatemer as size marker. Cleavage fragments are labeled alphabetically from largest to smallest for Ty2; homologous fragments in CT18 are labeled according to Ty2. Arrowheads indicate differences between the two strains. For example, there is no AvrII C band in CT18 because it is split into two parts in CT18 due to the inversion of I-CeuI A (see the inversion on the maps in "B"). Most of the other cleavage sites are conserved. (B) AvrII cleavage maps, with the previously constructed I-CeuI maps aligned to the AvrII maps to show the ends of the I-CeuI A inversion (i.e., rrnG and H).Among the 127 S. typhi strains analyzed including Ty2 and CT18, we resolved 22 genome types (GTs), from GTs 1 to 27, with GTs 10, 12, 15, 19, and 20 being predicted but not yet observed (table 1). Each GT was further divided into subtypes according to the orientations of I-CeuI A or I-CeuI C. As shown above, the main difference in genome structure between Ty2 and CT18 is the orientation of I-CeuI A; we arbitrarily assigned the Ty2 orientation of I-CeuI A as subtype a and the CT18 orientation as subtype b. Similarly, I-CeuI C in most S. typhi strains was oriented in the same way as in S. typhimurium LT2, which is true also for Ty2 and CT18; we assigned this I-CeuI C orientation as subtype c. Rarely, some S. typhi strains had the other I-CeuI C orientation and we assigned this as subtype d (table 1). These GTs could be grouped into three broad categories according to their severity of genome imbalance: (1) GTs 1–6 were most commonly observed (100 of 127 strains), with the genomes being 6° or less off balance; (2) GTs 7–24 were much less frequent (24 of 127 strains), with the genomes up to 31° off balance; and (3) GTs 25, 26, and 27 each had only one strain, with the genomes 55, 43, and 54° off balance, respectively. Figure 2 shows genome structures of representative strains for the three categories.
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Divergence of Genome Structure Within a Single S. typhi Strain
The requirement for a better balanced genome to keep an optimal bacterial growth rate and the availability of multiple homologous loci for recombination to facilitate genome rearrangement prompted us to speculate the presence, in a given S. typhi strain, of minority populations that might have genome structures different from that of the parent strain, with the potential to dominate if they were better balanced. We looked into this issue by starting a culture of CT18 with a single colony and streaking the culture onto LB plates. We picked up 100 colonies and mapped the bacterial genomes. We found that bacteria from three of the 100 colonies had different genome structures (fig. 3).
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These three CT18 derivatives, CT18-1, CT18-2, and CT18-3, all had inversions but at different loci, making the "net" balance status unchanged (CT18-2; note that the 6° off balance is on the other side of ori compared with the wild-type CT18) or worse (CT18-1 and CT18-3) relative to CT18. Among these three, CT18-1 and CT18-2 made colonies with indistinguishable morphology compared with the wild-type CT18, whereas CT18-3 made small colonies and its genome was very unbalanced. The fact that none of the three had a better balanced genome may explain why these CT18 derivatives did not become dominant, although we still believed that a derivative would increase in proportion in the population if it became better balanced (see Selection for Bacterial Cells with Better Balanced Genomes Under Stressed Conditions for supportive evidence). Such minority populations were also detected in many other S. typhi strains at very different frequencies, depending on how well the genome in the parental strain was balanced. For example, we did not find any rearrangement in S. typhi strains with genomes only 1–2° off balance; on the other hand, rearrangement was detected at high frequencies in strains with very unbalanced genomes, such as in SARB63, in which the genome was as much as 55° off balance (see below).
Selection for Bacterial Cells with Better Balanced Genomes Under Stressed Conditions
To further correlate high frequencies of genome rearrangement with high levels of genome imbalance, we applied a stressed condition, Caco2 epithelial cell invasion, on S. typhi to see whether we could detect higher frequencies of cells with better balanced genomes than that of the parent strain, assuming that cells with better balanced genomes would have better coordinated life activities considering more optimal growth rate as well as gene dosage factors in bacteria with better balanced genome (Liu and Sanderson 1995d). Remarkably, cells of SARB63 that passed the Caco2 monolayer exhibited a great diversity in colony size on LB plates (fig. 4A). SARB63 cells from colonies of different sizes had different genome structures, with those in larger colonies having better balanced genomes (fig. 4B).
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We assumed that, among the benefits that balanced genomes could render the bacteria, optimal time length for DNA replication might be most significant because any level of imbalance would result in extended replication time in one half of the genome between ori and ter. Growth curve analysis showed greatly shorter generation times in cells with better balanced genomes (table 2).
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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Different genome arrangements have a different ori-ter balance. The data presented here show that an ori-ter imbalance is associated with a reduced growth rate and that balanced GTs are more common in the S. typhi population. This supports the rearrangement-for-rebalancing model, which states that genome rearrangement might quickly become detectable in bacteria as they respond to genome balance-disturbing events and play a key role in rebalancing the genome. As most Salmonella lineages have the highly conserved S. typhimurium-type genome structure (Liu et al. 1999
), we presume that they already have a balanced genome and so do not need to rearrange it for better fitness. On the other hand, a number of Salmonella serovars have large insertions, and they usually also have rearranged genomes (Liu and Sanderson 1998; Liu et al. 2002), which is consistent with the model. In this regard, genome plasticity, or diversity of genome structure, in S. typhi could best be interpreted as the result of nonprecise balance restoration through rearrangements in the extant GTs, which points to a possibility that genome structure diversification by rearranging would become undetectable once precise genome balance has been reached in a line of cells and these cells would take over all S. typhi populations. In fact, we had seen such a case in another host-adapted Salmonella typhoid agent, S. paratyphi A (Liu and Sanderson 1995a). The genome of S. paratyphi A strain ATCC9150 has an increased size of DNA of about 100 kb in I-CeuI fragment A, which is about half of the genome, and this half genome is inverted compared with most Salmonella genomes. We postulated that this inversion in ATCC9150 might have helped rebalance the genome (Liu and Sanderson 1995a), and genomic sequencing has confirmed that this strain indeed has a balanced genome (McClelland et al. 2004). As the rearranging-for-rebalancing model would predict, S. paratyphi A does not exhibit diverse genome structures, and all analyzed wild-type strains of S. paratyphi A have the same genome structure (Liu and Sanderson 1995a). Analysis of genome rearrangement may help to trace the evolutionary route of a given bacterial lineage leading to a pathogen, capturing the specific events associated with acquisition of pathogenicity and change of host range. For example, characterization of specific genomic features of S. typhi may help elucidate the origins of typhoid pathogenesis and the molecular basis for strict host adaptation, providing insights into emergence of new pathogens and host-parasite interactions.
It is of interest to note another peculiar genome feature of S. typhi, that is, the relatively high copy number of the insertion sequence IS200, which exists in many Salmonella species and some Shigella species (Lam and Roth 1983, 1986; Gibert, Barbe, and Casadesus 1990; Gibert et al. 1991; Beuzon, Chessa, and Casadesus 2004). IS200 may provide homologous sites for recombination (Alokam et al. 2002) and its copy number may reflect its levels of activeness in genome rearrangements: S. typhimurium has only six copies of IS200 (Sanderson et al. 1993) and the genome structure is stable, whereas S. typhi has as many as 25 copies of IS200 (Parkhill et al. 2001), and the genome structure is highly plastic (Liu and Sanderson 1996). Two out of the three inversions in S. typhi CT18 derivatives shown in figure 3 were not in rrn genes and may possibly be mediated by IS200. Thus S. typhi, and perhaps also other host-adapted Salmonella, have both the need (to rebalance the genome) and the "facilities" (multiple copies of IS200 in addition to rrn operons to mediate homologous recombination) to rearrange the genome toward optimal fitness.
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Acknowledgements |
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This work was supported by an Natural Science Foundation of China grant (30370774), a 985 Project grant of Peking University Health Science Center, and a Discovery Grant from Natural Sciences and Engineering Research Council to S.L.L., a Canadian Institutes of Health Research grant to R.N.J., and an National Institutes of Health grant AI-34829 to K.E.S. W.Q.L. was supported by a summer studentship from Alberta Heritage Foundation for Medical Research.
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Footnotes |
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1 This paper is dedicated to the memory of Professor Sho-Xian Li, who deceased on November 21, 2004.
Jennifer Wernegreen, Associate Editor
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References |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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Alokam, S., S. L. Liu, K. Said, and K. E. Sanderson. 2002. Inversions over the terminus region in Salmonella and Escherichia coli: IS200s as the sites of homologous recombination inverting the chromosome of Salmonella enterica serovar typhi. J. Bacteriol. 184:6190–6197.
Beuzon, C. R., D. Chessa, and J. Casadesus. 2004. IS200: an old and still bacterial transposon. Int. Microbiol. 7:3–12.[ISI][Medline]
Blattner, F. R., G. Plunkett III, C. A. Bloch et al. (17 co-authors). 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453–1474.
Deng, W., S. R. Liou, G. Plunkett III, G. F. Mayhew, D. J. Rose, V. Burland, V. Kodoyianni, D. C. Schwartz, and F. R. Blattner. 2003. Comparative genomics of Salmonella enterica serovar Typhi strains Ty2 and CT18. J. Bacteriol. 185:2330–2337.
Doolittle, R. F., D. F. Feng, S. Tsang, G. Cho, and E. Little. 1996. Determining divergence times of the major kingdoms of living organisms with a protein clock. Science 271:470–477.[Abstract]
Feng, D. F., G. Cho, and R. F. Doolittle. 1997. Determining divergence times with a protein clock: update and reevaluation. Proc. Natl. Acad. Sci. USA 94:13028–13033.
Finlay, B. B., and S. Falkow. 1990. Salmonella interactions with polarized human intestinal Caco-2 epithelial cells. J. Infect. Dis. 162:1096–1106.[ISI][Medline]
Fleischmann, R. D., M. D. Adams, O. White, R. A. Clayton, E. F. Kirkness, A. R. Kerlavage, C. J. Bult, J. F. Tomb, B. A. Dougherty, J. M. Merrick et al. (40 co-authors). 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512.
Gibert, I., J. Barbe, and J. Casadesus. 1990. Distribution of insertion sequence IS200 in Salmonella and Shigella. J. Gen. Microbiol. 136(Pt 12):2555–2560.[Medline]
Gibert, I., K. Carroll, D. R. Hillyard, J. Barbe, and J. Casadesus. 1991. IS200 is not a member of the IS600 family of insertion sequences. Nucleic Acids Res. 19:1343.
Kohara, Y., K. Akiyama, and K. Isono. 1987. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell 50:495–508.[CrossRef][ISI][Medline]
Kothapalli, S., S. Nair, S. Alokam, T. Pang, R. Khakhria, D. Woodward, W. Johnson, B. A. Stocker, K. E. Sanderson, and S. L. Liu. 2005. Diversity of genome structure in Salmonella enterica Serovar typhi populations. J. Bacteriol. 187:2638–2650.
Krawiec, S., and M. Riley. 1990. Organization of the bacterial chromosome. Microbiol. Rev. 54:502–539.
Lam, S., and J. R. Roth. 1983. IS200: a Salmonella-specific insertion sequence. Cell 34:951–960.[CrossRef][ISI][Medline]
———. 1986. Structural and functional studies of insertion element IS200. J. Mol. Biol. 187:157–167.[CrossRef][ISI][Medline]
Liu, G. R., K. Edwards, A. Eisenstark, Y. M. Fu, W. Q. Liu, K. E. Sanderson, R. N. Johnston, and S. L. Liu. 2003. Genomic diversification among archival strains of Salmonella enterica serovar typhimurium LT7. J. Bacteriol. 185:2131–2142.
Liu, G. R., A. Rahn, W. Q. Liu, K. E. Sanderson, R. N. Johnston, and S. L. Liu. 2002. The evolving genome of Salmonella enterica serovar Pullorum. J. Bacteriol. 184:2626–2633.
Liu, S. L., A. Hessel, and K. E. Sanderson. 1993. Genomic mapping with I-Ceu I, an intron-encoded endonuclease specific for genes for ribosomal RNA, in Salmonella spp., Escherichia coli, and other bacteria. Proc. Natl. Acad. Sci. USA 90:6874–6878.
Liu, S. L., and K. E. Sanderson. 1992. A physical map of the Salmonella typhimurium LT2 genome made by using XbaI analysis. J. Bacteriol. 174:1662–1672.
———. 1995a. The chromosome of Salmonella paratyphi A is inverted by recombination between rrnH and rrnG. J. Bacteriol. 177:6585–6592.
———. 1995b. Genomic cleavage map of Salmonella typhi Ty2. J. Bacteriol. 177:5099–5107.
———. 1995c. I-CeuI reveals conservation of the genome of independent strains of Salmonella typhimurium. J. Bacteriol. 177:3355–3357.
———. 1995d. Rearrangements in the genome of the bacterium Salmonella typhi. Proc. Natl. Acad. Sci. USA 92:1018–1022.
———. 1996. Highly plastic chromosomal organization in Salmonella typhi. Proc. Natl. Acad. Sci. USA 93:10303–10308.
———. 1998. Homologous recombination between rrn operons rearranges the chromosome in host-specialized species of Salmonella. FEMS Microbiol. Lett. 164:275–281.[CrossRef][ISI][Medline]
Liu, S. L., A. B. Schryvers, K. E. Sanderson, and R. N. Johnston. 1999. Bacterial phylogenetic clusters revealed by genome structure. J. Bacteriol. 181:6747–6755.
McClelland, M., K. E. Sanderson, S. W. Clifton et al. (35 co-authors). 2004. Comparison of genome degradation in Paratyphi A and Typhi, human-restricted serovars of Salmonella enterica that cause typhoid. Nat. Genet. 36:1268–1274.[CrossRef][ISI][Medline]
McClelland, M., K. E. Sanderson, J. Spieth et al. (26 co-authors). 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852–856.[CrossRef][Medline]
Nair, S., S. Alokam, S. Kothapalli, S. Porwollik, E. Proctor, C. Choy, M. McClelland, S. L. Liu, and K. E. Sanderson. 2004. Salmonella enterica serovar Typhi strains from which SPI7, a 134-kilobase island with genes for Vi exopolysaccharide and other functions, has been deleted. J. Bacteriol. 186:3214–3223.
Ochman, H., and A. C. Wilson. 1987. Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J. Mol. Evol. 26:74–86.[CrossRef][ISI][Medline]
Parkhill, J., G. Dougan, K. D. James et al. (41 co-authors). 2001. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413:848–852.[CrossRef][Medline]
Sanderson, K. E., and M. Demerec. 1965. The linkage map of Salmonella typhimurium. Genetics 51:897–913.
Sanderson, K. E., P. Sciore, S. L. Liu, and A. Hessel. 1993. Location of IS200 on the genomic cleavage map of Salmonella typhimurium LT2. J. Bacteriol. 175:7624–7628.
Smith, C. L., J. G. Econome, A. Schutt, S. Klco, and C. R. Cantor. 1987. A physical map of the Escherichia coli K12 genome. Science 236:1448–1453.
Song, J., A. Ware, and S. L. Liu. 2003. Wavelet to predict bacterial ori and ter: a tendency towards a physical balance. BMC Genomics 4:17.[CrossRef][Medline]
Taylor, A. L., and M. S. Thoman. 1964. The genetic map of Escherichia coli K-12. Genetics 50:659–677.
Wong, K. K., and M. McClelland. 1992. A BlnI restriction map of the Salmonella typhimurium LT2 genome. J. Bacteriol. 174:1656–1661.
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